This paper tested different schemes for how the brain could represent
probabilities on owl’s auditory neurons: a population code where the
stimulus-driven activity and distribution of preferred stimuli in the
population represent a likelihood function and a prior; the sampling hypothesis
which proposes that the stimulus-driven activity over time represents a
posterior probability and that the spontaneous activity represents a prior; and
the class of models which propose that a population of neurons represents a
posterior probability in a distributed code. The spontaneous firing rate and
the average stimulus-driven response were not consistent with predictions of
the sampling hypothesis. In addition, neural activity under varying levels of
sensory noise did not reflect a posterior probability. Thus responses were only
consistent with the non-uniform population code model.

The study used the filtering properties of
the owl's head to predict the reliability of the timing cue used to localize
sounds in noisy environments. For each direction, there was a frequency range that carried the most
reliable cues. The study then showed a remarkable correlation between the
frequencies preferred by space-specific neurons and the range that carried the
most reliable cue for each direction. This paper is strong evidence indicating
that the brain is sensitive to statistics of sensory cues related to the
degree of uncertainty of the sensory input.

While the barn owl has been extensively used as a model for sound
localization and temporal coding, less is known about the mechanisms at its
sensory organ, the basilar papilla (homologous to the mammalian cochlea). This
paper characterized, for the first time in the avian system, the auditory nerve fiber responses to broadband noise using reverse correlation. The study showed that complex features such as the dependence of phase on input level, can still be consistent with simple linear filtering. This paper allows examining hypotheses put forward for mammalian cochlea.

Ascending the auditory
pathway, neurons increasingly show a preference for envelope modulation
frequencies. This study targeted a transition between auditory nerve fibers and
the cochlear nucleus. The paper linked spike threshold adaptation in
cochlear-nucleus neurons to their selectivity to modulation frequencies. Thus a
basic mechanism such as spike threshold adaptation could explain the enhanced
efficiency of envelope coding from the auditory nerve to the cochlear nucleus.

Space
specific neurons in the owl’s inferior colliculus are selective for motion
direction. We found that preference for sounds moving toward frontal space
increased with eccentricity in spatial tuning. This distribution was consistent
with larger receptive-field asymmetry in neurons tuned to more peripheral
auditory space. Directions that elicited larger response induced stronger
forward suppression on the response at subsequent locations along the sound’s
trajectory, thus making the response direction selective. The paper concluded
that response adaptation and receptive-field shape could explain direction
selectivity to acoustic motion and an orderly distribution of preferred
direction.

Space
specific neurons in the owl’s inferior colliculus are selective for motion
direction. We found that preference for sounds moving toward frontal space
increased with eccentricity in spatial tuning. This distribution was consistent
with larger receptive-field asymmetry in neurons tuned to more peripheral
auditory space. Directions that elicited larger response induced stronger
forward suppression on the response at subsequent locations along the sound’s
trajectory, thus making the response direction selective. The paper concluded
that response adaptation and receptive-field shape could explain direction
selectivity to acoustic motion and an orderly distribution of preferred
direction.

Interaural
level difference (ILD) is a critical cue for sound localization. ILD-detector
neurons in the owl’s lateral lemniscus (LLDp), equivalent to the mammalian LSO,
receive excitatory input from one side and inhibitory from the other. Here we
examined the spectrotemporal tuning of both type of inputs and how they
converge. We found that the firing of LLDp neurons is highly locked to the
stimulus envelope. The inhibitory input, acting as a gain modulator, enhances
the reliability of envelope coding in LLDp.

The owl’s midbrain contains a map of
auditory space where the front is overrepresented. This paper reports a
population-wide bias in the receptive fields of the neurons that constitute the
map, such that lateral suppression from frontal space was always stronger. The
findings could be predicted by a population of neurons with preferred
directions overrepresenting frontal space and exerting lateral inhibition on
each other. Thus, the uneven distribution of spatial tuning explained the
topography of an emergent tuning property.

Here we investigated the spectrotemporal
selectivity of monaural inputs in neurons that detect interaural time
difference (ITD). We found that these inputs are matched not just for frequency
but for frequency over time. A model based on cross-correlation showed that ITD
tuning depends strongly on this selectivity. We further showed that this
refinement could develop through spike timing-dependent plasticity. This paper
offered an alternative to how ITD tuning could be regulated.

This study
initiated a bottom-up approach to how the auditory system encodes stimulus
identity. Envelope coding was compared in the two cochlear nuclei of the barn
owl, nucleus angularis (NA) and nucleus magnocellularis (NM). We found that NA
neurons, although unable to accurately encode stimulus phase, lock more
strongly to the stimulus envelope than NM units. Further, we could relate the
shape of the spectrotemporal receptive fields to this enhanced tuning. These
findings suggest a dichotomy in envelope coding as early as at the first stage
in the central auditory pathway.

Owls
systematically underestimate peripheral source directions. This paper reports
that this behavior is predicted by a Bayesian model that emphasizes central
directions. It is proposed that a bias in the neural coding of auditory space
achieves high behavioral accuracy in the front at the cost of inducing errors
in the periphery. This bias was consistent with the overrepresentation of
frontal space observed in the map. This paper also reports that the properties
of the map and its neurons allow for a simple population vector to approximate
Bayesian inference.

This study focused on the modulation of spontaneous
neurotransmitter release by retrograde messengers in the chicken midbrain. Spontaneous
neurotransmitter release has been considered synaptic ‘noise’. Recent work,
however, suggested that these events could contribute to synaptic function. We
found that somatic depolarization suppressed spontaneous synaptic release onto chicken
midbrain neurons. These results indicated that these cells can specifically modulate
spontaneous neurotransmitter release of its afferent inputs in a retrograde
manner.

We built a model that accounted for the
emergence of spatial tuning in the owl’s midbrain. The model combined spatial
cues nonlinearly but linearly across frequency, as suggested by our
intracellular studies. This model provided two advances: First, it embraced the diversity of spiking
responses demonstrated experimentally; second, it reconciled multiplicative responses of spatial cues with
the presence of linear frequency integration.

This paper compared the spatial tuning in the
midbrain and the auditory thalamus. Thalamic cells respond to a broader
frequency range and their tuning to binaural cues varies more across frequency
than in the midbrain. The frequency dependence was enhanced by the
response to lower frequencies in the thalamus. Despite these differences, neurons in the thalamus could display spatial
receptive fields as selective as in the midbrain, suggesting that spatial
coding undergoes a change at the entryway to the forebrain.

An in
vitro preparation of the chicken midbrain was developed to study synaptic
plasticity in the avian auditory midbrain. We recorded neurons
in the external part of the auditory torus (EX). We studied the connection between EX cells and inputs originating in the midbrain.
Repetitive stimulation of these inputs induced LTD, a single-cell process
mediated by endocannabinoids. Endocannabinoids both decreased release
probability and reduced postsynaptic NMDA-receptor currents. This was the first report of eCB-dependent
LTD in the auditory midbrain.

Wild JM, Kubke MF, Peña JL (2008) A pathway
for predation in the brain of the barn owl (Tyto alba): projections of the
gracile nucleus to the "claw area" of the rostral wulst via the dorsal
thalamus. J. Comp. Neurol. 509:156-66.Pubmed

With our colleagues from Auckland, New
Zealand, we visited the owl’s somatosensory
system. The Wulst of
birds, is largely visual, but a relatively small rostral portion contains a representation
of the contralateral claw. We investigated whether the input to this “claw
area” arises from dorsal thalamic neurons that, in turn, receive their
somatosensory input from the gracile nucleus. Using retrograde and anterograde tracers we
found a trisynaptic pathway from the body periphery to the telencephalic Wulst,
via the dorsal thalamus. This pathway is likely involved in the barn owl’s
predatory behavior.

Interaural time difference (ITD) plays a
central role in sound localization. Theory
predicts that neurons that detect ITD behave as cross-correlators. While cross-correlation-like properties have
been reported, attempts to show that the shape of the ITD response function is
determined by the spectral tuning of these neurons, a core prediction of
cross-correlation, have been unsuccessful.
The paper demonstrates this relationship in neurons of the owl’s nucleus
laminaris, using reverse correlation to estimate the inputs from each side.

Neurons in the initial stages of the owl’s
auditory pathway phase lock to frequencies ass high as 8 kHz. However, phase
locking is rapidly abolished in a single-step transition. This paper reports
that despite two stages of convergence
and loss of phase information, the pathway preserves spectrotemporal
information in envelope-locked responses. It is also evidence of
simultaneous rate- and timing-based coding strategies representing multiple
stimulus parameters.

This article
showed that the brainstem of the barn owl realizes a processing analogous to
averaging. It showed that the signal-to-noise ratio in encoding of the
interaural time difference (ITD) abruptly increases from the place where it is
computed to the inferior colliculus (IC). The rate-ITD functions of IC neurons
require as little as a single stimulus presentation to show coherent tuning. Average-like
processes have been predicted by models of sound localization to remove noise.
These data support those predictions and address a recurrent them in
theoretical neuroscience.

Here we
tested if neural multiplication was tolerant to changes in the amplitude of one
input, as a mathematical multiplication should be. For this, we changed the
correlation of sound between the ears, which modulates the amplitude of one of
the two independent inputs to these cells. We found that the multiplication
remained, as predicted by the mathematical operation.

Comparison of subthreshold postsynaptic
potentials and spiking output of space-specific neurons recorded
intracellularly in vivo showed that subthreshold
receptive fields were much larger than those measured in spikes. The main cause
of these changes was the strategic location of the spiking threshold. In addition,
the thresholds of the spikes at the beginning of a sound were lower than those
of later sound-induced spikes and of spontaneous spikes due to dependence
between the spiking threshold and the preceding change in membrane potential.
This phenomenon could account for the sharpening of ITD selectivity from the
beginning to end of the stimulus.

The space-specific neurons of the owl showed
one of the cleanest examples of multiplication by systems of neurons.
Multiplication is a powerful processing tool that, if implemented by the brain,
would explain the emergence of neural combination selectivity. The owl’s
auditory system computes interaural time (ITD) and level (ILD) differences to
create a two dimensional map of auditory space. A multiplication of separate inputs
tuned to ITD and ILD could account for the response of these neurons to ITD-ILD
pairs. This finding lent support not just to models of sound localization but
also to the use of multiplication to describe combination selectivity by
neurons.

This paper tested predictions of two
alternative models of ITD detection: one that takes into consideration
differences in wave propagation along the cochlear basilar membrane
(“stereausis theory”) and another one that uses neural delays (“Jeffress
model”). We showed that for the owl there is no need to invoke mechanisms other
than neural delays to explain the detection of ITD.

Here we
reported intracellular in vivo recordings
in the owl’s inferior colliculus for the first time. We studied how frequencies
converge onto these cells to resolve the ambiguity inherent to the periodic
nature of sound. The paper reports a largely sublinear integration across
frequency and a central role of spiking threshold in disambiguating the
response.